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Preservation Methods Influence Human Lateral Menisci Biomechanical Properties. An ex-vivo Comparative
Study of Three preservation methods (Freezing, Cryo-preservation and Freezing+Irradiation).
Christophe Jacquet, Roger Erivan, Akash Sharma, Martine Pithioux, Jean-Noël Argenson, Matthieu Ollivier
To cite this version:
Christophe Jacquet, Roger Erivan, Akash Sharma, Martine Pithioux, Jean-Noël Argenson, et al.. Preservation Methods Influence Human Lateral Menisci Biomechanical Properties. An ex-vivo Comparative Study of Three preservation methods (Freezing, Cryo-preservation and Freezing+Irradiation).. Orthopaedic Journal of Sports Medicine, SAGE Publications, In press,
�10.1007/s10561-013-9396-7�. �hal-02042618�
1 2 3 4 5 6
C. Jacquet, R. Erivan, A. Sharma, M. Pithioux, S. Parrattte, J.N. Argenson, M. Ollivier 7
8 9
Preservation Methods Influence Human Lateral Menisci Biomechanical Properties.
10
An ex-vivo Comparative Study of Three preservation methods (Freezing, Cryo- 11
preservation and Freezing+Irradiation).
12 13 14 15 16 17 18 19 20 21 22 23 24 25
ABSTRACT.
26
Backgrounds: Three main menisci preservation methods have been used over the last 27
decade: freezing, freezing with gamma-irradiation, and cryopreservation.
28
Hypothesis/Purpose: We hypothesized that all preservation methods will result in similar 29
biomechanical properties as defined by traction and compression testing.
30
Methods: Twenty-four human lateral menisci were collected from patients operated on for 31
total knee arthroplasty. The inclusion criteria were patients under 70 years of age, with 32
primary unilateral (medial) femorotibial knee osteoarthritis. Cross sectionally each meniscus 33
was divided into 2 specimens extending from the end of the central edge peripheral/capsular 34
attachment to obtain 2 similar samples from the same meniscus. One sample was 35
systematically cryopreserved constituting the control group (Cy;-140°c) and the other was 36
used for either the simple frozen group (Fr;-80°c ) or the frozen + irradiated group (FrI;-80°c 37
+ 25kGy irradiation).
38
Evaluation was performed using compression and tensile tests (Instron 5566 Universal 39
Testing Machine) to analyze: 1) the Elasticity Modulus (Young’s Modulus; YM) in 40
compression, 2 )the YM in traction, 3)the Tensile Force at failure, 3)the Rupture Profile of the 41
tensile stress-strain curve.
42
Results: A significant difference of the mean compression elasticity’s modulus was observed 43
between Cy group and the Fr group (respectively 28.86±0.77MPa vs 37.26±1.08MPa; mean 44
difference 8.40±1,33MPa; p <0,001) and between the Cy group and the FrI group 45
(respectively 28.86±0.77MPa vs 45.92±1.09MPa; mean difference 17.06±1.33MPa;
46
p<0,001).
47
A significant difference of the mean tensile elasticity’s modulus was observed between Cy 48
group and the Fr group (respectively 11.66±0.97MPa vs 19.97±1.37MPa; mean difference 49
8.31±1.68MPa; p=0.008) and between the Cy group and the FrI group (respectively 50
11.66±0.97MPa vs 45.25±1.39MPa; mean difference 33.59±1.59MPa; p<0,001).
51
We did not find any significant difference regarding the Tensile Force at failure between the 52
different groups.
53
The analysis of stress-strain curve between groups revealed a slow-slope curve with a non- 54
abrupt rupture (ductile material) for cryopreserved samples. A clear rupture of the stress- 55
strain curve was observed for frozen and frozen + irradiated samples (more fragile material).
56
Conclusion: We rejected our hypothesis that all preservation methods will result in similar 57
biomechanical properties. Cryopreservation allows to obtain a more elastic and less fragile 58
tissue than the simple freezing or freezing plus irradiation.
59 60
Key Words: Meniscus; Allograft ; Conservation ; Storage ; Irradiation ; 61
Cryopreservation ; Freezing ; Mechanical Properties.
62 63
Clinical relevance: The results of our study exhibit detrimental effect of simple freezing and 64
freezing+irradiation on Human menisci’s mechanical properties. If those effects occur in 65
menisci prepared for allograft procedure, important differences could appear on graft’s 66
mechanical behavior and thus patients’ outcomes.
67 68
What is known about the subject: Three main menisci preservation methods have been 69
advocated: freezing, freezing with gamma-irradiation, and cryopreservation Gamma.
70
Cryopreservation is the only method that preserves fresh meniscus architectural specificities.
71
Freezing and freezing+irradiation methods modify histological properties of meniscal 72
allograft. The results of those procedure have been not “directly” compared using adapted 73
mechanical testing, in the actual literature.
74 75
What this study adds to existing knowledge:
76
Our study compared the three main preservations methods on identical samples using two 77
different mechanical testings, aiming to approximate in-vivo loading.
78
Our results, first, confirmed that Freezing+Irradiation procedure should be used with caution, 79
second, demonstrated that Freezing also have a detrimental effect on menisci mechanical 80
properties, third, allowed us to conclude that Menisci Tissues preserved using 81
Cryopreservation result in better mechanical outcomes.
82 83 84
INTRODUCTION.
85
The long-term damaging effects of total meniscectomy include: pain, potential 86
instability and osteoarthritis 12,13,16. Menisci allografts have been advocated to treat these 87
issues and potentially slow the onset of osteoarthritis. Mid-term results of this procedure 88
demonstrate significant improvement in patient’s pain scores 26,27, as well as increasing 89
survivorship without failure (85%) of meniscal allografts10,28. To play its biomechanical role, 90
meniscus allograft tissue must resemble the qualities of native fibrocartilage25. As such, graft 91
preservation methods will play a vital role in the biological, mechanical and thus clinical 92
success of menisci allograft techniques5. Three main menisci preservation methods have been 93
used over the last decade: freezing, freezing with gamma-irradiation, and cryopreservation25. 94
In a recent comparative study Jacquet et al 14 observed that Cryopreservation does not 95
cause significant histological alterations as compared to fresh tissue. On the other hand, 96
significant differences were only found comparing between freezing and freezing with 97
irradiation processes to fresh tissue or cryopreserved samples.
98
These ex-vivo microscopic findings need to be validated to estimate their clinical implication.
99
This biomechanical study was designed to compare “preserved menisci allografts”
100
mechanical properties defined by the elasticity’s modulus during traction and compression 101
testing, as there is nothing in the literature to confirm that preserving meniscal architecture 102
preserves the biomechanical properties of the graft. We hypothesized that all preservation 103
methods will result in similar biomechanical properties.
104 105 106
METHODS.
107
Following local board approval, twenty-four human lateral menisci were collected 108
from patients operated on for total knee arthroplasty from September to October 2017. All 109
patients gave written consent prior to their inclusion into the study. Inclusion criteria were:
110
patients aged <70 years undergoing Total Knee Arthroplasty with isolated medial femoral- 111
tibial arthritis or femoral-patellar and medial femoral-tibial joint degeneration (but with an 112
lateral femoral-tibial compartment graded Kellgrenn and Lawrence <2 15) and no history of 113
prior surgery, trauma, or developmental disease of the operated knee. An MRI was 114
systematically performed 1 month pre-operatively to verify the absence of radiological 115
meniscal lesion. If a grade 1 lesion was detected, the patients were not included in the study 116
Patient’s characteristics are summarized in Table 1.
117 118 119 120 121 122 123 124 125
126 127 128 129 130
131 132 133
134 135 136 137 138
Patients Age (yr) Gender Weight
(kg)
Height (cm)
BMI (kg.m-2)
01 63 M 77 182 23.2
02 65 M 82 186 23.7
03 61 F 68 175 22.2
04 64 F 56 158 22.4
05 66 M 84 186 24.3
06 67 M 79 181 24,1
07 60 M 77 184 22.7
08 59 F 63 161 24.3
09 64 M 79 178 24.9
10 62 F 57 159 22.5
11 63 F 61 164 24,3
12 61 F 63 165 22.7
13 67 F 62 164 23.1
14 63 F 56 159 22.2
15 62 M 74 182 22.3
16 69 M 77 179 24.0
17 68 M 79 180 24.4
18 62 M 77 177 24.6
19 62 F 63 162 24.0
20 64 F 59 167 21.2
21 67 M 73 177 23.3
22 68 F 64 164 23.8
23 67 M 80 180 24.7
24 61 F 68 169 23.8
Table 1 Patient’s characteristics
BMI : body mass index
Figure 1 : Series' flow-chart Cy : cryopreservation
Fr : Frozen 139
140 141 142 143 144 145 146 147 148 149 150 151 152 153
Samples Preparation 154
Cross sectionally each meniscus was divided into 2 specimens extending from the end of the 155
central edge peripheral/capsular attachment to obtain 2 similar segments, one superior and 156
one inferior (Figure 1). One sample was systematically cryopreserved constituting the control 157
group (Cy) and the other was used for either the simple frozen group (Fr) or the Frozen + 158
Irradiated group (FrI), Figure 1. The choice of the sample among the superior and inferior 159
fragments was done randomly for each group.
160
For compression testing a parallelepiped specimen was harvested from each sample to obtain 161
parallel flat surfaces at the central region of the meniscus (Fgure 2). Tensile testing did not 162
require further preparation. Each sample was measured with a digital caliber (Absolute 163
Digimatic solar, Mitutoyo, resolution U = 0,01 mm) and only underwent tensile or 164
compression testing.
165 166 167 168 169 170
171 172 173 174 175 176 177 178
Meniscus samples were plunged into a physiological saline solution and then placed in a 179
cryo-kit (8°C) for transportation to the local tissue bank (<6 hours). Specimens were prepared 180
with the following steps: (1) graft reception in clean room (controlled atmosphere zone); (2) 181
decontamination of the graft with an antibiotic solution (Rifampicin + Thiophenicol); (3) 182
rinsing with 0.1M cacodylate buffer for 5 min; and (4) bacteriological sampling. Following 183
preparation, different conservation methods were applied. 1) For the cryopreservation group 184
cryoprotective solution (10% of DMSO + SCOT 30 were added, the bag was vacuumed to 185
extract the residual air, and progressively decreased the temperature (Starting at -4°C then 186
decreasing at -2°C per minute to -40°C and then -5°C per minute to -140°C). Samples were 187
stored in a nitrogen tank in a vapor phase at -145°C. 2) For the frozen group, a simple 188
Figure 2 Sample’s preparation for the compression tests
freezing process was used, progressively decreasing the temperature (starting at -4°C then 189
decreasing at -2°C per minute to -40°C and then -5°C per minute to -80°C). 3) For the frozen 190
+ irradiated group, a simple congelation with a progressive decrease in temperature (starting 191
at -4°C then decreasing at -2°C per minute to -40°C and then -5°C per minute to -80°C) was 192
performed. The grafts were then transported in a dry ice-controlled container (stored at -80°C) 193
to be irradiated by gamma-rays by IONISOS factory ©. The doses received ranged between 194
22.7 and 27.8 kGy (2.2-2.7 Mrad). After this treatment, the samples were again stored at - 195
80°C until analysis was undertaken. All samples were Stored at least 1 month prior to 196
biomechanical testing 197
198
Biomechanical Testing 199
The compression and tensile tests were performed on an Instron 5566 Universal Testing 200
Machine with a measurement error in displacement of 0.05% and the force transducer has a 201
measurement error of 0.2% in tension and compression.
202 203
Compression test (Figure 3).
204
Each sample was subjected to 5 relaxation compression cycles with a maximum load of 50 N.
205
The speed of progression was 3mm / min.
206
The Stress-strain curve was then obtained using pre-test relaxed measurement of section and 207
thickness. Elasticity Modulus (Young’s Modulus) was calculated in the relaxation elastic 208
phase of the 5th cycle 23. 209
210 211 212 213
214 215 216 217 218 219 220 221 222 223 224 225 226 227
Tensile test (Figure 4) 228
Each sample was attached to the ends of the tensile testing machine by jaws dedicated to 229
handle soft tissue to prevent inadvertent movement (INSTRON 2716_015, force max 30kN 230
with jaw face 0-0.25/25T/IN) 21. The positioning required 1/3 of the specimens’ length in each 231
jaw, the central 1/3 defining the initial length (L0) before traction. An increasing load (10 mm 232
/ min) was applied until the specimens’ failed. A stress-strain curve was obtained for each 233
specimen using the dimensions of the samples. Then, we calculated Young’s modulus in the 234
elastic phase of the testing curve. Moreover, tensile force at failure was noted.
235 236 237 238
Figure 3 compression test
239 240 241 242 243 244 245 246 247 248 249 250
Statistics 251
Prior to the initiation of the study a sample analysis estimated that 6 samples for each group 252
will be necessary to be powered (80%) to distinguish ∆: 5±3 nm Young’s modulus values.
253
Patients characteristics were expressed using the appropriate descriptive statistics for the type 254
of variables. Descriptive statistics included mean with SD, or median with interquartile range, 255
as appropriate, for continuous variables. The Student t tests were used to compare the 256
distribution of continuous parameters between groups (or the Mann-Whitney test when the 257
data were not normally distributed or when the homoscedasticity assumption was rejected).
258
All reported p values were 2- sided, with a significance threshold of \.05. Statistical analysis 259
was performed using SPSS/JMP software (version 13; Microsoft software).
260
261 262
Figure 4 Tensile test
Compression test (Table 2) 264
265
266
Table 2 Compression Elasticity's Modulus (Young's modulus) 267
MPa: MegaPascal 268
269 270 271
A significant difference of the mean compression elasticity’s modulus was observed between 272
Cy group and the Fr group (respectively 28.86 ± 0.77 MPa vs 37.26 ± 1.08 MPa; mean 273
difference 8.40 ± 1,33 MPa and p <0,001).
274
A significant difference of the mean compression elasticity’s modulus was also found 275
between the Cy group and the FrI group (respectively 28.86 ±0.77 MPa vs 45.92 ± 1.09 MPa;
276
mean difference 17.06 ± 1.33 MPa and p<0,001) 277
278 279 280 281 282 283 284 285 286
Absolute value of Mean difference (MPa)
IC-95% (MPa) P value
Cryopreserved Frozen 8.40 5.40-11.41 p<0.001
Cryopreserved Frozen + irradiated 17.06 14.05-20.07 p<0.001
Tensile test (Table 3-4) 287
288
289
290 291
A significant difference of the mean tensile elasticity’s modulus was observed between Cy 292
group and the Fr group (respectively 11.66 ± 0.97 MPa vs 19.97 ± 1.37 MPa; mean difference 293
8.31 ± 1.68 MPa with p = 0.008) 294
A significant difference of the mean tensile elasticity’s modulus was also noticed between the 295
Cy group and the Fr group (respectively 11.66 ± 0.97 MPa f vs 45.25 ± 1.39 MPa; mean 296
difference 33.59 ± 1.59 MPa with p<0,001) , Table 4.
297 298 299 300
301 302 303 304
Absolute value of Mean difference (MPa)
IC-95% (MPa) P value
Cryopreserved Frozen 8.31 4.50-12.12 p=0,008
Cryopreserved Frozen+ irradiated 33.59 29.78-37.39 p<0.001
Table 3 Tensile Elasticity’s modulus N: Newton
Absolute value of Mean difference (N)
IC-95% (N) P value
Cryopreserved Frozen 78.33 16.02-131.33 p=0.186
Cryopreserved Frozen + irradiated 40.50 28.95-107.25 p=0.1993
Table 4 Force at Failure N: Newton
305 306
With the number available we did not find any significant difference regarding Force at 307
failure between the different groups, the mean difference being 78.3N IC95% 16.02-131.33
308
between cryopreserved and frozen specimens (p=0.186) and 40.5 IC95% 28.95-107.25 and 309
between cryopreserved and Frozen+Irradiated specimens (p=0.199) (Table 4) 310
The analysis of stress-strain curve between groups revealed a slow-slope curve with a non- 311
abrupt rupture (ductile material) for cryopreserved samples (Figure 5A). A clear rupture of the 312
stress-strain curve was observed for frozen and frozen + irradiated samples (more fragile 313
material) (Figure 5B).
314
In addition, failure seemed to happen quicker for the frozen storage and frozen + irradiated 315
specimens than in cryopreserved samples where the failure was more gradual, which is most 316
probably due to the delamination of the fibers.
317 318 319 320 321 322 323 324 325 326 327 328
329
Figure 5A Stress-strain curve of a cryopreserved sample 330
331 332 333 334 335 336 337 338 339 340 341 342 343 344 345 346 347 348 349 350 351 352 353
0 0,5 1 1,5 2 2,5 3 3,5 4
0 0,2 0,4 0,6 0,8 1 1,2
Str ess (MP a)
Strain
354 355 356
Figure 5B Stress-strain curve of a frozen sample 357
358 359 360
. 361 362 363 364 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382
0 0,5 1 1,5 2 2,5 3 3,5 4 4,5 5
0 0,1 0,2 0,3 0,4 0,5
Str ess (MP a)
Strain
DISCUSSION 383
384 385
The key finding of this study is that Cryopreservation allows for more elastic and less fragile 386
tissue than the simple freezing or freezing plus irradiation. We rejected our hypothesis that all 387
preservation methods will result in similar biomechanical properties. We observed a 388
significant change in the Young’s modulus in both compression and traction testing when 389
comparing Cryopreserved and Frozen specimens. These findings were more obvious when 390
comparing differences between Cryopreserved and Frozen + irradiated specimens. All of our 391
findings might be explained by an increased rigidity of the meniscal tissue related to the 392
freezing and/or irradiation procedures.
393
The relatively large variability in tensile and compression stiffness amongst different 394
preservation processes is multifactorial. In general, the tensile mechanical properties of 395
biological materials depend on the relative contents of major extracellular matrix constituents, 396
the organization of the matrix constituents and the interactions of these constituents meniscal.
397
Prior studies have reported that different preservation methods can alter meniscal 398
ultrastructure 8,9, which corroborates the differences we saw between cryopreservation, 399
freezing and freezing + irradiation.
400
Whilst conducting this study we were also able to examine the meniscal Tensile Force at 401
Failure and rupture profile of the tensile strain- curve. This is also defined as the ability of 402
collagen tissue to absorb energy until it fractures. The Tensile Force at Failure of the Frozen 403
and Frozen + irradiated samples were lower than for cryopreserved samples even if this 404
difference was not statistically significant. This decrease in Tensile Force at failure could 405
lead to more frequent lesions of Frozen and Frozen + irradiated grafts during transverse 406
stresses occurring during flexion-extension movements.17. 407
Our analysis of the stress-strain curves demonstrates that the cryopreserved meniscal tissue 408
has a very gradual rupture profile reflecting a “ductile material”, where Frozen and Frozen + 409
irradiated samples, present an acute rupture often found in “fragile material”. This means that 410
cryopreserved samples have the ability to deform without breaking at higher absorbed energy 411
levels than frozen samples and frozen + irradiated samples during extreme traction 20. 412
No data was found in the literature with regards to estimating the elasticity’s modulus of fresh 413
meniscus (in compression or traction), or the force at failure.
414
Regarding tensile elasticity modulus, the available data is summarized in the table 5.
415 416
Mean tensile elasticity’s modulus (MPa) Bursac et Al 2009 2
Frozen specimen from deceased donor Storage time: not disclosed
80.9 ± 24.6 20.3-129.1
Tissackh et Al 24 1995
Frozen specimen from deceased donor Storage time: not disclosed
72.85 ± 22.91 3.59-151.80
Ahmad et Al 2017 1
Frozen specimen from living donor Storage time: 6 weeks
54.17 ± 19.54 NC
Table 5 summary of available data for the tensile elasticity modulus 417
418
Our values are slightly lower than elastic moduli presented in similar published literature.
419
Those differences can be explained by the fact that most of the studies 2,24, utilized samples 420
harvested from deceased donors without any information on the sampling sequences and the 421
storage time. In our study, all samples were from living donors. In order to limit the 422
deleterious effects of prolonged exposure to ambient temperature, the samples were 423
immediately placed in a Cryo-kit at 8 ° C and the preservation process was carried out in less 424
than 6 hours 7. Using tissue from living donors instead of cadaveric tissue avoids bias related 425
to death-induced hypoxia which could adversely affect the biomechanical tissue properties 19. 426
In Ahmad et Al Study 1, meniscus samples came from a patient with a tumor near the knee 427
whom required a prosthetic replacement. No information was disclosed regarding possible 428
radiotherapy treatment received, which would likely modify the biomechanical properties of 429
the meniscus. In these three studies 1,2,24 no information was provided on the freezing process 430
utilized, in particular the rate of descent of temperature, which has been described as a factor 431
that may cause tissue damage 22. 432
For compression testing, the only data identified from the literature comes from Chia et Al’.s 433
study3 which described a highly variable Young’s Modulus (between 0,135 and 1,130 MPa) 434
according to the preconditioning strain level (3%, 6%, 9% or 12% strain). In this study only 435
ten cadaveric medial menisci were studied (in our study we only considered lateral menisci).
436
The authors did not indicate the time between death and freezing, the existence of 437
degenerative or traumatic pathology, or the freezing process used. These differences may 438
contribute and explain the greater variability of these published results in comparison to our 439
conducted study.
440
One of the limitations of our study is the lack of fresh tissue group. However, it was 441
impossible to obtain three different samples from the same meniscus because the amount of 442
material was insufficient to perform the mechanical tests. More, testing fresh tissue suppose 443
to be able to create and attach specimens into the loading device before tissue’s ischemia. We 444
did not found solutions in the actual literature to avoid this limitation. Most of the authors 445
freezed their specimens before testing and do not estimate fresh tissue properties.
446
We recognize another limitation of our study, the mean age of our patients in which 447
specimens were harvested were in comparison older than donors in others studies (average 448
age 63.8 years in our study versus 53,5 in the register 4). Because of this, menisci evaluated 449
during our analyses might have been altered by aging and degenerative processes. We tried to 450
avoid limitation related to this methodological bias by excluding menisci with significant 451
MIR’s lesion and studying only non-arthritic joints (lateral compartment) from subjects 452
suffering from only medial femoral-tibial degeneration. It’s also described by Bursac et Al2 453
that there are no significant correlations, between either the biochemical composition or the 454
tensile mechanical properties and donor age of lateral or medial menisci. . Another difficulty 455
encountered in this study was the creation of 2 samples from the same meniscus. Although 456
there is no data in the literature that asserts that the superior and inferior parts of a meniscus 457
have different biomechanical properties, we have randomly assigned each fragment (superior 458
or inferior) in each group to limit this potential bias.
459
Finally, our study only approximates the physiological biomechanical environment of the 460
meniscus. The compression tests simulate the loading of the meniscus during walking and 461
thus its ability to absorb axial shocks during several loading cycles 6,11. But the compression 462
forces are not distributed uniformly over the entire surface of the meniscus and essentially 463
only concerns the middle segment18. Our tensile tests simulate the transverse stresses applied 464
to the horn-root junction of the meniscus during flexion-extension movements 29. But in-vivo 465
tensile strains are predominantly located at the root-horn junction, where the meniscus is 466
adherent to the tibial plate29. We tried to reproduce this anatomical representation by placing 467
the fixed point of the jaws at the ends of the menisci, near the insertion of the roots. During 468
weightbearing and movement, the menisci are normally subjected to a combination of 469
tension, compression, and shear forces. Shear forces could not be evaluated in this study 470
because no device allowed to reproduce in vitro the impact of these forces. Thus, the ability of 471
a meniscal allograft to withstand these forces after transplantation would appear to be a key 472
element in the successful outcome of such a procedure.
473 474
475
CONCLUSION 476
Cryopreserved meniscal sections demonstrated superior stress-strain, tension, and 477
compression biomechanics compared to frozen and frozen+ irradiated specimens.
478
Cryopreservation allows preservation of an elastic and less fragile meniscal allograft than 479
freezing and the freezing + irradiation process.
480 481 482 483 484
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